Introduction Insect Herbivores Cactus Hosts
Classification of Cactus-Feeding Insects Host Specificity of Cactus-Feeding Insects Insect Adaptations to Their Cactus Hosts Endophagous Herbivores and Survival External Herbivores Insect Pests on Cultivated Cacti Distribution of Pests Predicting Future Pests Diseases of Cultivated Cacti Bacteria Yeasts Fungi
Native Fungi on Cacti Other Diseases Conclusions and Future Prospects Literature Cited
One of the earliest published records of a cactus-feeding insect dates back to Alexander von Humboldt in 1812 (Ortega 1991), who described how the cochineal insect Dactylopius coccus had been cultivated in Mexico and Central America for many centuries before the arrival of Columbus. Between 1877 and 1895, several other publications mentioned insects feeding on cacti in the United States. The most comprehensive work on insects of Cactaceae, published at the beginning of the last century, was The Principal Cactus Insects of the United States by Hunter et al. (1912), which lists 324 species, including species from Mexico and Central America, 92 of which are recorded as being injurious to cacti.
Early research into the biological control of alien cactus invaders in countries such as Australia, India, and South Africa made a significant contribution to the study of cactus-feeding insects. Indeed, several cacti, including various species in the genera Cylindropuntia, Harrisia, Opuntia, and Pereskia from North and South America, have become serious invaders and have been subjected to biological control programs (Dodd 1940; Pettey 1948; Annecke and Moran 1978; Moran and Zimmermann 1984; Julien and Griffiths 1998; Olckers and Hill 1999). As a result, many papers were published on the taxonomy, bi ology, and ecology of selected natural enemies used to control these cactus weeds biologically (Blanchard 1922; Cockerell 1929; Dodd 1940; Pettey 1948; De Lotto 1974; Moran and Cobby 1979; Robertson 1987; Robertson and Hoffmann 1989; Hoffmann 1991). Some of these insects are now important pests of cultivated Opuntia species.
The most significant research contributions on cactus-feeding insects resulted from the comprehensive surveys made by various entomologists in their search for effective biocontrol agents (e.g., Mann 1969; Zimmermann et al. z979). These studies focused primarily on the subfamily Opuntioideae (Cylindropuntia, Opuntia, Tephrocactus) with some information also on Pereskia and Harrisia of subfamilies Pereskioideae and Cactoideae, respectively. Very little is known of the insects associated with other genera, particularly those in the Pereskioideae and Cactoideae, because very few of their species have become invaders outside of their natural habitats. The only such species that have become invasive outside the Americas are Cereus jamacaru, Harrisia martinii, and Pereskia aculeata. Had the whole of the Cactaceae been studied as comprehensively as the Opuntioideae, the number of recorded cactus-feeding insect species would certainly be much larger. Also, the cactus-feeding insects of the Caatinga region of Brazil, as well as those of Paraguay and Bolivia, are un-dersampled and there are many undescribed species in these regions (Mann 1969). Only limited surveys have been undertaken of the subfamily Pereskioideae, mainly in Argentina (Zimmermann et al. 1979).
Early surveys of cactus pathogens are unknown, most likely because diseases were not considered for biological control of cactus weeds at that stage. The first noteworthy publications on cactus diseases came from North America, where the emphasis was on commercially cultivated ornamentals and native species (Alcorn et al. 1975; Mitchell 1985). Farr et al. (1989) list 10 fungus species causing disease symptoms for Opuntia ficus-indica. Most of the important information on cactus diseases is derived from studies of pathogens in the Mediterranean countries, where diseases cause considerable damage to cultivated plantings comprised mainly of O. ficus-indica and its many cultivars. Many of the diseases are polyphagous and are well known from other crops. Some, mainly in Mexico, have now spread from native cactus species to those in cultivation.
Compared to other plant families, relatively few cactus-feeding insects have co-evolved with the Cactaceae (Moran
1980). This may be attributed to the unique morphology and physiology of the family. The insects that do feed on succulent Cactaceae usually have co-evolved with their hosts and have special features and adaptations that allow them to survive on these hosts. The main driving force in the evolution of the Cactaceae was the selection for features that reduce desiccation. This resulted in morphological and physiological changes, such as succulence (80-90% water), Crassulacean acid metabolism (CAM; Chapter 4), a large diversity of alkaloids, abundance of oxalic acid, loss of leaves, decreased surface/volume ratios, mucilage, and a tough cuticle (Benson 1982; Barthlott and Hunt 1993). Many cactus-feeding insects have overcome these barriers and have adapted in unique ways to these drastic changes.
The complexity of plants is correlated with the number of insect species associated with them, and the Cactaceae are for the most part architecturally simple— generally no leaves, hairs, or trichomes (Lawton and Schroder 1977; Strong and Levin 1979). These traits, together with the reduced niche space, could have contributed to the reduced but highly host-specific insect fauna observed in the Cactaceae. This is another reason why so few phytophagous insects worldwide have been able to adapt to introduced Cactaceae outside the Americas. In comparison, the evolution of cactus diseases is rapid, because the biochemical characteristics of cactus cells adapt well to the various disease agents' requirements. Thus, epidemics caused by diseases are able to spread rapidly, causing extensive damage to large commercial cactus-pear plantations.
In the known cactus-feeding insect community some families, such as the Pyralidae (pyralids) and the Cerambycidae (long-horned beetles), are over-represented, while other important insect families are lacking (Fig. 14.1). The pyralids are most numerous with approximately 58 species feeding on cacti, followed by the cerambycids with 33 species, and the Curculionidae (weevils) with about 20 species. The family Dactylopiidae (cochineals; Chapter 13) is unique to Cactaceae (Fig. 14.1) and all of its nine species are specific to the Opuntioideae, with the exception of Dactylopius con-fertus, which lives on a Cleistocactus sp. (De Lotto 1974). The family Cactaceae hosts only one species from the family Diaspididae (scale insects), namely Diaspis (Diplacaspis) echinocacti; this species is host specific to the family. The total absence of the large insect families, such as the Noctuidae (noctuid moths) and Pentatomidae (shield bugs), is astonishing, as cacti should be particularly attractive to these insects. The absence of specific and naturally
(pyralids) (long-horned (weevils) (twig wilters) (flies) (cochineals) taxa beetles)
(pyralids) (long-horned (weevils) (twig wilters) (flies) (cochineals) taxa beetles)
Figure 14.1. The number of cactus-feeding insects in North and South America out of a total of 165 species. Data partially from Moran (1980).
occurring cactus fruit flies (Tephritidae) is equally astonishing in view of the large diversity of fruit found within the Cactaceae. Some of the common fruit flies, which are generalist pests on cultivated fruit worldwide, e.g., Ceratitis cap-itata, have recently switched to Opuntia fruit. Moran (1980) showed that, for both North and South America, more insect species feed on the larger opuntias than on the smaller, narrow-jointed ones, which is consistent with the typical species/area relationship of phytophagous insects (Strong 1979).
The differences in the number of insect taxa of North and South American cactus floras suggest a long period of isolation among the cactus-feeding faunas. In particular, very few insect taxa are shared. Second, the large diversity of insects and mites associated with the northern region suggests that most cacti evolved in North America. Specifically, 35% more cactus-feeding species occur in North America than in South America. The small number of cur-culionid and cerambycid species from South America (Fig. 14.1) is surprising, but more surveys in South America probably will not reveal many more new species that might change this imbalance. The Coreidae (squash bugs) are represented in North America by two large genera, Chelinidea and Narnia, which are absent from South America. Instead, in South America the Coreidae are represented by the small genus Leptoglossus, one of the genera found in both the Americas. The Lonchaeidae (lonchaeid flies) are well represented in South America, as opposed to only two species in North America. Their larvae feed internally in the cladodes of mainly Opuntia species.
A fascinating feature of the family Pyralidae is that the larvae of all true cactus-feeding members of the family in South America are reddish, whereas those in North America are blueish, except Ozamia and Sigelgaita, which vary in color. These aposematic (warning) colors suggest a defense strategy against predators, although which poisonous larvae they mimic is not known. All members of the genera Ozamia and Sigelgaita, as well as the only species in the genus Noctuella in family Pyraustidae (pearl moths), are primarily fruit feeders and occasionally destroy large proportions of fruit (Mann 1969). Ozamia species occur in both North and South America, whereas the other two genera are found only in South America. Some of the Ozamia fruit-feeding species are associated with a wide host range in both the Opuntioideae and Cactoideae. Because of their ability to consume fruits, it is surprising that these insects are not more serious pests on cultivated Opuntia species.
The dominance of internal cladode feeders (Fig. 14.2) within the major insect families associated with Cactaceae may be an indication of the advantages of endophagy. The succulent internal environment, in addition to the tough, thick, wax-covered epidermis typical of the Cactaceae, provides excellent protection. About 75% of all cactus-feeding
Leaf miner 1%
Free-living sap -| suckers 9%
Free-living sap -| suckers 9%
insects and mites are internal feeders and only 3% of the species feed externally (Fig. 14.2). The rest are fruit feeders and sap suckers. Even though only a few insects have been collected from the subfamily Pereskioideae (Zimmermann et al. 1979), which contains the primitive, leaf-bearing cactus species, its insect guild differs clearly from that of the other two subfamilies. It is characterized by a higher incidence of external feeders and leaf-miners, which may be attributed to the presence of prominent leaves.
According to Mann (1969), about 80% of the species of cactus-feeding insects are found in genera of which all members are restricted to cactus hosts, indicating a high degree of host-plant specialization. On the other hand, within the Cactaceae, very few cactus-feeding insects are mono-phagous, i.e., restricted to a single host species, such as Dactylopius salmianus, which is found only on Opuntia salmianus. Most cactus-feeding insects are oligophagous, i.e., restricted to a single genus. A few are restricted to a subfamily. For example, species in the Pyralidae and the Dactylopiidae are mainly associated with the genus Opuntia within the Opuntioideae, whereas the Cerambycidae feed on all three subfamilies.
Distinct insect complexes are associated with the sometimes-invoked genera Platyopuntia and Cylindropuntia of the Opuntioideae, as defined by Backeberg (1976), which might be regarded as evidence in favor of retaining these genera. From western Texas to California, three insects species—the moth borers (Pyralidae) Cahela ponderosella and Alberada parabates, and the cerambycid Coenopaeus palmeri—are all associated with Cylindropuntia, including the widely distributed Opuntia imbricata. According to Mann (1969), all attempts to rear the two pyralids on Platyopuntia were unsuccessful, whereas the cerambycid was able to develop on Opuntia species when forced by restrictive cage conditions. Species within the large genus Narnia also show very clear preferences for either Platy-opuntia or Cylindropuntia, and the cochineal, Dactylopius tomentosus, is associated only with Cylindropuntia. Equally, under natural conditions Cactoblastis cactorum is only associated with Platyopuntia, although under caged condition it can develop on some Cylindropuntia. This specificity between insects and host plants can have important implications for cactus taxonomists. It can also be a valuable tool for predicting the future pest status of some of these insects for the large commercial cactus-pear plantations within the insects' native ranges.
Recent studies reveal host-adapted biotypes within certain cactus-feeding insect species. Two distinct, host-adapted biotypes exist in the cochineal Dactylopius opun-tiae. One of the biotypes attacks only large, tree-like Opuntia species, such as Opuntia ficus-indica, whereas the other is restricted to low-growing Opuntia species, such as the O. stricta types in North America (Githure et al. 1999; Volchansky et al. 1999). This implies that certain Opuntia weeds can be controlled biologically, using a host-specific cochineal biotype, without threatening the commercial plantations of O. ficus-indica. The existence of host-adapted biotypes within the cochineals also has important implications for the biological control of other Opuntia weeds. Furthermore, host-adapted biotypes may exist within the commercially cultivated Dactylopius coccus, which could have far-reaching consequences for the cochineal industry. In fact, preliminary research suggests that carmine cochineal populations may differ in their host-plant preferences (Robles 1999).
The pyralid moth, Cactoblastis cactorum (Fig. 14.3), has a very wide host range within the genus Opuntia and has been recorded as developing on at least 29 hosts (Zimmermann et al. 2000). Many of its hosts within the North American opuntias constitute new associations and are being controlled very effectively by C. cactorum. Also, the pyralid is able to develop on all six native Opuntia species within their native range in Florida (Johnson and Stiling 1998). This spells disaster to many native opuntias in all of mainland North America if the insect arrives there (Zimmermann et al. 2000). The damage caused by C. cactorum to cultivated Opuntia species in Mexico, should it arrive
there, could be substantial. In any case, McFadyen (1985) recognized ten biotypes of C. cactorum, based on larval differences, host plants, and locality records. Host-adapted biotypes are likely to be found in several other cactus insects, including the Coreidae, e.g., Narnia species.
Cactus-feeding insects have adapted to the succulence, thick cuticle, and other characteristics that are highly developed within the Cactaceae as adaptations to a xero-phytic habitat. These characteristics may explain why insects indigenous to other continents have been unable to adapt successfully to this plant family, members of which have been introduced into those continents as ornamentals, crops, or invaders. The only exceptions are some polyphagous mealybugs, aphids, grasshoppers, and other opportunistic feeders. Opuntia ficus-indica, for instance, has been in South Africa for at least 260 years without accumulating any indigenous phytophages, although the time available has certainly been more than adequate and its distribution is wide enough (Moran 1980). More astonishing, none of the native, cactus-feeding insects living on the nearly 160 cactus species in Chile (including one na tive Opuntia species) has permanently switched to the large commercial plantations of O. ficus-indica in that country. This indicates that cactus-feeders have a high degree of host specificity, which is rare among other introduced crop plants, as shown in a study of crop plants and their insect pests in South Africa (Moran 1983).
Nearly 80% of all insects feeding on opuntias bore within the succulent plant tissues during the larval stages. This en-dophagy protects them against predators and parasitoids. The oviposition habits recognized among the cactus-feeding Lepidoptera are also aimed at reducing predation and parasitism, and all show close adaptations to their cactus hosts (Hoffmann and Zimmermann 1989). The most common method, used by the many species in the genera Cactoblastis and Melitara, entails the female moth depositing her eggs—one on top of the other—in the form of an eggstick that superficially resembles a spine. The larvae hatch simultaneously and enter the cladode collectively through one entrance hole. By entering the cladode more rapidly, the larvae can avoid the mucilage secretions that often repel small larvae (Robertson and Hoffmann 1989). Single, first-instar larvae of Cactoblastis cactorum are deterred from penetrating cladodes successfully by the secretions; even if they do manage to enter, it takes longer than when they enter gregariously through a single entrance hole (Hoffmann and Zimmermann 1989). In other pyralids, such as Tucumania and members in the Pyraustidae (e.g., Megastes, Metapleura, and Mimorista), which deposit their eggs singly on thorns or directly on the surface of their hosts, egg mortality is higher than in eggstick-producing species (Hoffmann and Zimmermann 1989). The larvae of all the pyralids are endophagous and are well protected from predators and parasitoids. They are brightly colored in the later instars when they venture out of the cladodes to pupate, suggesting a possible aposematic function. Some members of the Pyralidae are important pests on cultivated Opuntia species (Longo and Rapisarda 1995).
Many Opuntia species grow in warm, semiarid regions where air and soil temperatures can reach levels of 49°C and 65°C, respectively. For most plants, temperatures over 54°C are lethal, even if they last only a short period (Nobel 1988). Temperatures inside the cladodes of Opuntia species are even higher, because lack of daytime stomatal opening associated with CAM prevents water loss and therefore cooling of the surface (Chapter 4). A temperature of 59°C has been measured inside a cladode when the air temperature was only 43°C (Went 1982). How the endophagous pyralid larvae survive these temperatures is not known. In
South Africa, C. cactorum larvae have been observed leaving the protection of their cladodes during very hot spells, possibly to avoid the high internal temperatures (Pettey 1948). Such exposure drastically increases the chances for predation.
Carminic acid (Chapter 13) acts as a potent feeding deterrent to parasitoids and ants (Eisner et al. 1980). Nonetheless, two species in the Pyralidae, Laetilia coccidivora from North America and Salambona analamprella from South America, are uniquely adapted to act as both predators of the cochineals and as phytophages. Their larvae are free-living and tunnel in cladodes underneath cochineal colonies. For self-protection, the larvae of L. coccidivora sequester carminic acid from the cochineals on which they prey (Mann 1969; Eisner et al. 1980) and can severely harm the commercial rearing of Dactylopius coccus in Mexico (Tito 1998). In any case, sequestering poisons for self-protection is common in insects that feed on poisonous plants.
With the exception of two chrysomelid (leaf beetles) species that feed externally on young cladodes, the larvae of all cactus-feeding species in the Coleoptera (beetles) — notably families Curculionidae and Cerambycidae—are endophagous and thus well protected from parasitoids and predators. Females deposit their eggs individually on the plant in scar tissue or in cracks and crevices, which are then covered with a secretion that hardens to provide protection. The presence of larvae is revealed by frass (debris produced by insects) or gum and/or mucilage exudations. Some of the major pests on cultivated Opuntia species are in these two families. The adult cerambycids are all very cryptic and difficult to detect when resting on the bark of their cactus hosts.
Apart from the polyphagous species in the Miridae (mirid bugs), e.g., Hesperolabopspicta, all known cactus-feeding sap suckers (Fig. 14.2) in the Heteroptera (bugs) belong to family Coreidae (squash bugs). These are seldom abundant, with the exception of Chelinidea species that can develop pest status on cultivated Opuntia species in Mexico (Gallegos Vazquez and Mendez Gallegos 2000), causing yellowing around feeding punctures. Most of these sap suckers feed gregariously. At the least disturbance, they move quickly to the protected side of the cladode and with continued disturbance, they drop to the ground to find cover. They are vulnerable to predation and parasitism and have evolved no special protection mechanisms, apart from their rapid movements and the repugnancy typical of coreids.
The most extraordinary insects that have co-evolved with the Cactaceae are the nine species of the genus Dactylopius of the Dactylopiidae (cochineals; De Lotto 1974; Chapter 13). They are all sedentary, and the females are protected by a thick waxy covering and the carmine in their body fluids that gives the insect its typical red color. The behavior and life cycles of Dactylopius austrinus, D. coccus, D. opuntiae, and D. tomentosus have been studied in detail (Dodd 1940; Pettey 1948; Karny 1972; Moran and Cobby 1979; Moran et al. 1982; Hosking 1984; Perez Guerra and Kosztarab 1992; Chapter 13). The insects feed in an exposed position on the surface of the cladodes and are vulnerable to excessive rain, which washes them off the plant. Moran et al. (1987) and Moran and Hoffmann (1987) highlighted adaptations in the insect to avoid excessive damage caused by rain, such as settling in the rain shadow of a cladode or near the protection of a spine. Predators, mainly coccinellid beetles, are well adapted to prey on cochineal in their countries of origin. Predators that have not co-evolved with the insects are less effective due to the deterrent effect of carmine and because of the waxy covering that provides effective protection to the insect (Morrison 1984).
Dactylopius austrinus, D. ceylonicus, D. opuntiae, and D. tomentosus have all been used successfully in the biological control of cactus weeds in many countries, and they are rated as one of the most effective groups of biocontrol agents (Zimmermann and Moran 1982; Moran and Zimmermann 1984; Julien and Griffiths 1998). Why these cochineals are so damaging to their hosts is not known. Some of the hosts, e.g., Opuntiaficus-indica, can support large populations of D. coccus without being obviously affected.
Cactus-feeding insects can apparently detect the CO2 gradient associated with the plant's CAM activity and use it to their own advantage. The moth Cactoblastis cactorum detects small fluctuations in CO2 around the background atmospheric levels, enabling females to recognize the healthiest and physiologically most active plants (Stange et al. 1995). Cactophagous insects probably have other adaptations to the CAM pathway, such as the effect of the daily acidity fluctuations associated with CAM.
Insect Pests on Cultivated Cacti
Considering the number of recorded cactus-feeding insects and mites, only a few of these species have become pests on cultivated Cactaceae, mainly Opuntia species (Longo and Rapisarda 1995). Little is known of the pests of the other commercially cultivated genera— Cereus, Hylocereus, Selen-icereus, and Stenocereus. By far the largest number of pests are recorded from Mexico, where Opuntia species are extensively cultivated (Table 14.1). This is not surprising, as Mexico is home to more than 150 native cactus-feeding insects and also the origin of many cultivated Opuntia species (Bravo 1978; Scheinvar 1999). Of the total of 122 specialist Opuntia-feeding species listed by Mann (1969) and Zimmermann et al. (1979), only 23 are general pests of cultivated Opuntia species in Mexico (Tito 1998; Gallegos Vazquez and Mendez Gallegos 2000).
Very few insect pests have been recorded on cultivated cacti in countries other than Mexico, including the Mediterranean countries. The cactus-feeding pests recorded from southern Africa, Australia, Madagascar, and India (Table 14.1) were deliberately introduced for biological control of Opuntia weeds (Moran and Zimmermann 1984; Brutsch and Zimmermann 1995). Except for very poly-phagous, opportunistic feeders, such as grasshoppers, aphids, ants, and mealybugs, no record could be found of a permanent host-switch onto cultivated Opuntia species from any of the native phytophagous insects in countries outside of North and South America. No insect pests have been recorded from cactus pear in Israel (Y. Mizrahi, personal communication). This is an indication of the taxo-nomic isolation and the uniqueness of the Cactaceae. Only recently has the introduced Mediterranean fruit fly, Ceratitis capitata, been recorded as a pest of fruit of Opuntia ficus-indica in South Africa. The only host-specific cactus-feeding insect that has followed the spread of cactus cultivations around the world is the scale insect Diaspis echinocacti. Because of the geographical isolation of the Cactaceae, no insect pest of any significance, apart from D. echinocacti, has been recorded from Ethiopia, where cactus-pear plantings cover many thousands of hectares along with the large areas of naturalized populations (Behailu and Tegegne 1997).
Opuntia species (Chapter 10) and, to a lesser extent, other species in the genera Hylocereus, Selenicereus, and Stenocereus (Chapter 11) are widely cultivated in many countries. The insect pests on Opuntia species vary considerably, depending on the country and the continent in which they are cultivated (Table 14.1). The pests in these countries will be divided into three geographic areas, beginning with North and South America. Countries in these regions, especially in North America, have the highest diversity of insect pests. These are native species that have transferred to cultivations and differ from North to South America. In Argentina, Cactoblastis cactorum is by far the most serious pest (Ochoa de Cornelli et al. 1992), but it is absent from
Brazil (Pernambuco) because of slow dispersal from its native range in Argentina, Uruguay, and Paraguay (G. P. de Arruda, personal communication). Many major pests are found in Mexico (Table 14.1), including Anastrepha species (Tephritidae), Cactophagus (Metamasius) species (Curculi-onidae), Chelinidea species (Coreidae), Cylindrocoptorus species (Curculionidae), Dactylopius species (Dactylopi-idae), Olycella and Laniifera species (Pyralidae), and Serico-thrips species (Thripidae; Gallegos Vazquez and Mendez Gallegos 2000). Several minor pests are also present.
The second area includes southern Africa, Mauritius, Australia, India, and some West Indian islands (Table 14.1). These are countries that have deliberately introduced Cactoblastis cactorum, Dactylopius opuntiae, and other insect species (Julien and Griffiths 1998) for the biological control of various Opuntia weeds (Moran and Zimmermann 1984). In most cases, the control is successful. The former two insects are now pests on cultivated O. ficus-indica and its cultivars, and control measures against them are necessary for successful cultivation of cactus pear (Annecke et al. 1976). The host-specific mealybug (Pseudo-coccidae) Hypogeococcus festerianus and the cerambycid beetle Alcidion cereicola were introduced into Australia and South Africa for the biological control of Harrisia martinii and Cereusjamacaru (Julien and Griffiths 1998). Both of these insect species will become pests should these countries decide to develop C. jamacaru as a commercial crop, as is the case in Israel (Mizrahi and Nerd 1999). Although the curculionid beetle Cactophagus (Metamasius) spinolae has been released as a biocontrol agent against O. ficus-indica in South Africa and is now well established and effective at one locality in the Eastern Cape, it has not yet dispersed to cultivated plantations of O. ficus-indica. This insect has the potential to become a serious pest on cultivated cactus pear plantations in South Africa.
Mediterranean countries, Ethiopia, the Canary Islands, Iran, and Iraq have very few pests on cultivated Opuntia species (Longo and Rapisarda 1995; Table 14.1). First, the pests were not transferred together with the plants at the time of introduction from their countries of origin; second, these countries had no biological control projects against invading Opuntia species; and third, no native insects transferred to Opuntia hosts. Some opportunistic feeders are occasionally found causing temporary damage to plants in these countries. The cactus scale insect, Diaspis echino-cacti, is the only insect that followed the introductions of Opuntia species throughout the world and is now found wherever such species are grown. A noncactus pest that has recently started causing damage to cultivated fruit in many countries, including South Africa and those in the
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